Clim. Past, 16, 1007–1025, 2020 https://doi.org/10.5194/cp-16-1007-2020 © Author(s) 2020. This work is distributed under the Creative Commons Attribution 4.0 License. Can morphological features of coccolithophores serve as a reliable proxy to reconstruct environmental conditions of the past? Giulia Faucher1, Ulf Riebesell2, and Lennart Thomas Bach3 1Dipartimento di Scienze della Terra “Ardito Desio”, Università degli Studi di Milano, Milan 20133, Italy 2Biological Oceanography, GEOMAR Helmholtz Centre for Ocean Research Kiel, Kiel 24105, Germany 3Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, Tasmania, Australia Correspondence: Giulia Faucher ([email protected]) Received: 9 July 2019 – Discussion started: 15 July 2019 Revised: 16 April 2020 – Accepted: 6 May 2020 – Published: 9 June 2020 Abstract. Morphological changes in coccoliths, tiny cal- changing light intensity, Mg=Ca ratio, nutrient availability, cite platelets covering the outer surface of coccolithophores, and temperature in terms of coccolith morphology. The lack can be induced by physiological responses to environmental of a common response reveals the difficulties in using coc- changes. Coccoliths recovered from sedimentary successions colith morphology as a paleo-proxy for these environmen- may therefore provide information on paleo-environmental tal drivers. However, a common response was observed un- conditions prevailing at the time when the coccolithophores der changing seawater carbonate chemistry (i.e., rising CO2), were alive. To calibrate the biomineralization responses of which consistently induced malformations. This commonal- ancient coccolithophore to environmental changes, studies ity provides some confidence that malformations found in the often compared the biological responses of living coccol- sedimentary record could be indicative of adverse carbonate ithophore species with paleo-data from calcareous nannofos- chemistry conditions. sils. However, there is uncertainty whether the morpholog- ical responses of living coccolithophores are representative of those of the fossilized ancestors. To investigate this, we 1 Introduction exposed four living coccolithophore species (Emiliania hux- leyi, Gephyrocapsa oceanica, Coccolithus pelagicus subsp. Coccolithophores are calcifying marine phytoplankton and braarudii, and Pleurochrysis carterae) that have been evo- are among the most important calcifiers in the ocean (Tyrrell lutionarily distinct for hundreds of thousands to millions of and Young, 2009). They produce single calcitic platelets years, to a range of environmental conditions (i.e., changing named coccoliths and nannoliths. Due to their ability to light intensity, Mg=Ca ratio, nutrient availability, tempera- calcify, coccolithophores played an important role in rock- ture, and carbonate chemistry) and evaluated their responses formation during the Jurassic and Cretaceous as well as in coccolith morphology (i.e., size, length, width, malforma- through the Cenozoic (e.g., Erba, 2006). They are directly tion). The motivation for this study was to test if there is affected by environmental drivers such as temperature, salin- a consistent morphological response of the four species to ity, nutrient concentration, light, and carbonate chemistry changes in any of the tested abiotic environmental factors. If that can modify physiological rates and morphology of cer- this was the case, then this could suggest that coccolith mor- tain taxa (e.g., Paasche, 1998; Riebesell et al., 2000; Langer phology can serve as a paleo-proxy for that specific factor et al., 2006; Trimborn et al., 2007; Zondervan et al., 2007; because this response is conserved across species that have Rosas-Navarro et al., 2016). Due to their sensitivities to been evolutionary distinct over geological timescales. How- environmental changes fossil remains of coccolithophores ever, we found that the four species responded differently to (coccoliths and nannoliths) have often been used as paleo- proxies to reconstruct past physical and chemical conditions Published by Copernicus Publications on behalf of the European Geosciences Union. 1008 G. Faucher et al.: Can morphological features of coccolithophores serve as a reliable proxy? in the surface ocean of local or global significance (e.g., In order to investigate our hypothesis outlined above, we Erba, 1994; Lees et al., 2005; Tiraboschi et al., 2009; Erba selected four different coccolithophore species: Emiliania et al., 2010, 2019; Lübke and Mutterlose, 2016; Faucher et huxleyi (morphotype R), Gephyrocapsa oceanica, Coccol- al., 2017a; S1 in the Supplement). To calibrate the biomin- ithus pelagicus subsp. braarudii, and Pleurochrysis carterae. eralization responses of ancient coccolithophorid algae to According to “molecular-clock-data”, they are evolutionarily climatic changes, studies often compared the biological re- distinct since the Triassic or the Jurassic (with the exception sponses of living coccolithophore species with paleo-data of G. oceanica and E. huxleyi, which diverged ∼ 290 Kya; from calcareous nannofossils (Table 1). Liu et al., 2010; Bendif et al., 2014). We present data on The primary goal of our study was to understand if phys- how coccolith size and morphology change in response to a iological experiments with contemporary species are a valid suite of different environmental drivers and explore whether tool to predict responses of ancient coccolithophores to en- there is a common response to any of these drivers among vironmental change in the geological record. The assump- the different species. Afterwards, we discuss if morphologi- tion that modern species respond identically to environmen- cal features of coccoliths have the potential to serve as paleo- tal change as ancient species did is implicit in many stud- proxies. ies (e.g., Giraud et al., 2006; Erba et al., 2010; Faucher et al., 2017a, Table 1) but, to the best of our knowledge, has 2 Material and methods not been explored in depth. To test this assumption, we did a series of identical stress test experiments with four se- 2.1 Experimental setup lected modern species that have been evolutionarily distinct for hundreds of thousands to millions of years (Fig. 1). Our Five experiments are presented in this study with a similar hypothesis was as follows: in the case that coccolith mor- design. Every experiment tested the influence of one abiotic phology responses to a changing environmental driver are parameter on four different coccolithophore species which similar in the four species, this could be indicative of a re- were cultured individually (i.e., in separate bottles). The sponse pattern that was physiologically conserved over ge- tested abiotic factors were as follows: light intensity, nutrient ological timescales because the species were evolutionarily limitations (N or P limitations), Mg=Ca ratio, temperature, separated for so long. In other words, if species conserve and carbonate chemistry. Monospecific cultures of the coc- a similar response to certain types of environmental change colithophores Emiliania huxleyi (strain RCC 1216, from the for geological timescales, despite very different evolutionary Tasmanian sea), Gephyrocapsa oceanica (strain RCC 1303, trajectories, then this would strengthen our confidence that from the French coast of the Atlantic Ocean), Coccolithus responses recorded for modern species also apply for the ge- pelagicus subsp. braarudii (strain PLY182G; it will be called ological past. hereafter C. braarudii, from the English Channel, Atlantic Indeed, there is considerable uncertainty when trying to Ocean), and Pleurochrysis carterae (unknown strain num- reconstruct paleo-environmental conditions based on coccol- ber, coastal species) were grown in artificial seawater (Kester ith morphology. This in itself is not surprising considering et al., 1967) under dilute batch culture conditions (LaRoche that there are millions of years of evolution between the et al., 2010). The artificial seawater medium was enriched time when the fossil coccolithophores lived and when the with 64 µmol kg−1 nitrate, 4 µmol kg−1 phosphate to avoid physiological experiments were done (Bown, 2005; De Var- nutrient limitations with the exception of the nutrient lim- gas et al., 2007). Moreover, for the fossil record, it is ex- itation experiment (see Sect. 2.1.3). In all experiments we tremely difficult to disentangle the individual factor(s) that added f=8 concentrations of vitamins and trace metals (Guil- −1 drove changes in coccolith morphology. Therefore, it is un- lard and Ryther, 1962), 10 nmol kg of SeO2 (Danbara and surprising that studies occasionally come to different conclu- Shiraiwa, 1999), and 2 mL kg−1 of natural North Sea water sions about what environmental factor drove a morphological to provide potential nutrients which were not added with the change in the paleo-record. For example, Erba et al. (2010), nutrient cocktail (Bach et al., 2011). The medium was sterile- detected the reduction in size and variation in shape of some filtered (0.2 µm). The carbonate chemistry was adjusted with nannofossil species during a time of excess volcanogenic aeration for 24 h using a controlled CO2 gas mixing system CO2 emissions. They explained their trend with detrimental reaching the treatment levels of f CO2 400 µatm (total alka- carbonate chemistry conditions based on physiological incu- linity, TA, 2302 µmol kg−1) with the exception of the carbon- bation studies by Riebesell et al. (2000) who found decreas- ate chemistry